Discrimination against the cytosine analog tC by escherichia coli DNA polymerase IV DinB

Journal of Molecular Biology

Volumn 409, Issue 2, 2011, Pages 89-100

  Walsh, Jason M ^a   Bouamaied, Imenne ^b   Brown, Tom ^b   Wilhelmsson, L Marcus ^c   Beuning, Penny J ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

major groove; primer extension; translesion synthesis; tryptophan fluorescence binding assay

Indexed keywords

1,3 DIAZA 2 OXOPHENOTHIAZINE; CYTOSINE DERIVATIVE; DEOXYGUANOSINE TRIPHOSPHATE; DNA POLYMERASE; DNA POLYMERASE IV; PROTEIN DINB; UNCLASSIFIED DRUG;

ARTICLE; DNA REPLICATION; DNA STRAND; ESCHERICHIA COLI; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING;

ESCHERICHIA COLI;

EID: 79955891559     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.069     Document Type: Article

References (76)

1. Kornberg A., and Baker T.A. DNA Replication 2nd edit. 1992 W. H. Freeman & Company New York, NY
2. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenbereger T. DNA Repair and Mutagenesis, 2 2006 ASM Press Washington, DC
3. McCulloch S.D., and Kunkel T.A. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases Cell Res. 18 2008 148 161
4. Jarosz D.F., Beuning P.J., Cohen S.E., and Walker G.C. Y-family DNA polymerases in Escherichia coli Trends Microbiol. 15 2007 70 77 (Pubitemid 46199189)
5. Sutton M.D., and Walker G.C. Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination Proc. Natl Acad. Sci. USA 98 2001 8342 8349 (Pubitemid 32678033)
6. Yang W. Portraits of a Y-family DNA polymerase FEBS Lett. 579 2005 868 872 (Pubitemid 40361856)
7. Ohmori H., Friedberg E.C., Fuchs R.P., Goodman M.F., Hanaoka F., and Hinkle D. The Y-family of DNA polymerases Mol. Cell 8 2001 7 8 (Pubitemid 32772900)
8. Ling H., Boudsocq F., Woodgate R., and Yang W. Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication Cell 107 2001 91 102 (Pubitemid 32972040)
9. Yang W. Damage repair DNA polymerases Y Curr. Opin. Struct. Biol. 13 2003 23 30 (Pubitemid 36170251)
10. Boudsocq F., Kokoska R.J., Plosky B.S., Vaisman A., Ling H., and Kunkel T.A. Investigating the role of the little finger domain of Y-family DNA polymerases in low fidelity synthesis and translesion replication J. Biol. Chem. 279 2004 32932 32940 (Pubitemid 39014753)
11. Beese L.S., Derbyshire V., and Steitz T.A. Structure of DNA polymerase I Klenow fragment bound to duplex DNA Science 260 1993 352
12. Steitz T.A. DNA polymerases: structural diversity and common mechanisms J. Biol. Chem. 274 1999 17395 17398
13. Steitz T.A., Beese L., Freemont P.S., Friedman J.M., and Sanderson M.R. Structural studies of Klenow fragment: an enzyme with two active sites Cold Spring Harb. Symp. Quant. Biol. 52 1987 465 471 (Pubitemid 18262356)
14. Tang M., Pham P., Shen X., Taylor J.S., O'Donnell M., Woodgate R., and Goodman M.F. Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis Nature 404 2000 1014 1018 (Pubitemid 30243598)
15. Yang W., and Woodgate R. What a difference a decade makes: insights into translesion DNA synthesis Proc. Natl Acad. Sci. USA 104 2007 15591 15598 (Pubitemid 350035345)
16. Washington M.T., Carlson K.D., Freudenthal B.D., and Pryor J.M. Variations on a theme: eukaryotic Y-family DNA polymerases Biochim. Biophys. Acta 1804 2010 1113 1123
17. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function Annu. Rev. Biochem. 74 2005 317 353 (Pubitemid 40995510)
18. Wagner J., Gruz P., Kim S.R., Yamada M., Matsui K., Fuchs R.P., and Nohmi T. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis Mol. Cell 4 1999 281 286 (Pubitemid 29456897)
19. 2-dG adduct are bypassed by different lesion-bypass DNA polymerases in E. coli DNA Repair (Amsterdam) 5 2006 515 522
20. Napolitano R., Janel-Bintz R., Wagner J., and Fuchs R.P. All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis EMBO J. 19 2000 6259 6265
21. 2-(1-carboxyethyl)-2′-deoxyguanosine by DinB DNA polymerase in vitro and in vivo Proc. Natl Acad. Sci. USA 105 2008 8679 8684 (Pubitemid 351987740)
22. Jarosz D.F., Godoy V.G., Delaney J.C., Essigmann J.M., and Walker G.C. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates Nature 439 2006 225 228 (Pubitemid 43083146)
23. Bellon S., Gasparutto D., Saint-Pierre C., and Cadet J. Guanine-thymine intrastrand cross-linked lesion containing oligonucleotides: from chemical synthesis to in vitro enzymatic replication Org. Biomol. Chem. 4 2006 3831 3837 (Pubitemid 44536097)
24. Minko I.G., Yamanaka K., Kozekov I.D., Kozekova A., Indiani C., and O'Donnell M.E. Replication bypass of the acrolein-mediated deoxyguanine DNA-peptide cross-links by DNA polymerases of the DinB family Chem. Res. Toxicol. 21 2008 1983 1990
25. Kumari A., Minko I.G., Harbut M.B., Finkel S.E., Goodman M.F., and Lloyd R.S. Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV J. Biol. Chem. 283 2008 27433 27437
26. Suzuki N., Ohashi E., Hayashi K., Ohmori H., Grollman A.P., and Shibutani S. Translesional synthesis past acetylaminofluorene-derived DNA adducts catalyzed by human DNA polymerase kappa and Escherichia coli DNA polymerase IV Biochemistry 40 2001 15176 15183 (Pubitemid 33151932)
27. Kobayashi S., Valentine M.R., Pham P., O'Donnell M., and Goodman M.F. Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment J. Biol. Chem. 277 2002 34198 34207
28. Stengel G., Gill J.P., Sandin P., Wilhelmsson L.M., Albinsson B., Norden B., and Millar D. Conformational dynamics of DNA polymerase probed with a novel fluorescent DNA base analogue Biochemistry 46 2007 12289 12297 (Pubitemid 350022383)
29. Sandin P., Stengel G., Ljungdahl T., Borjesson K., Macao B., and Wilhelmsson L.M. Highly efficient incorporation of the fluorescent nucleotide analogs tC and tCO by Klenow fragment Nucleic Acids Res. 37 2009 3924 3933
30. Marquez L.A., and Reha-Krantz L.J. Using 2-aminopurine fluorescence and mutational analysis to demonstrate an active role of bacteriophage T4 DNA polymerase in strand separation required for 3′ → 5′-exonuclease activity J. Biol. Chem. 271 1996 28903 28911 (Pubitemid 26382591)
31. Reha-Krantz L.J. The use of 2-aminopurine fluorescence to study DNA polymerase function Methods Mol. Biol. 521 2009 381 396
32. Sinkeldam R., Greco N., and Tor Y. Fluorescent analogs of biomolecular building blocks: design, properties, and applications Chem. Rev. 110 2010 2579 2619
33. Wilhelmsson L.M. Fluorescent nucleic acid base analogues Q. Rev. Biophys. 43 2010 159 183
34. Engman K.C., Sandin P., Osborne S., Brown T., Billeter M., and Lincoln P. DNA adopts normal B-form upon incorporation of highly fluorescent DNA base analogue tC: NMR structure and UV-Vis spectroscopy characterization Nucleic Acids Res. 32 2004 5087 5095 (Pubitemid 39445495)
35. Sandin P., Wilhelmsson L.M., Lincoln P., Powers V.E., Brown T., and Albinsson B. Fluorescent properties of DNA base analogue tC upon incorporation into DNA-negligible influence of neighbouring bases on fluorescence quantum yield Nucleic Acids Res. 33 2005 5019 5025 (Pubitemid 41487809)
36. Wilhelmsson L.M., Holmen A., Lincoln P., Nielsen P.E., and Norden B. A highly fluorescent DNA base analogue that forms Watson-Crick base pairs with guanine J. Am. Chem. Soc. 123 2001 2434 2435 (Pubitemid 32904782)
37. Lin K.Y., Jones R.J., and Matteucci M. Tricyclic 2′-deoxycytidine analogs-syntheses and incorporation into oligodeoxynucleotides which have enhanced binding to complementary RNA J. Am. Chem. Soc. 117 1995 3873 3874
38. Lin K.Y., and Matteucci M. A cytosine analogue capable of clamp-like binding to a guanine in helical nucleic acids J. Am. Chem. Soc. 120 1998 8531 8532 (Pubitemid 28420483)
39. Wilds C.J., Maier M.A., Tereshko V., Manoharan M., and Egli M. Direct observation of a cytosine analogue that forms five hydrogen bonds to guanosine: guanidino G-clamp Angew. Chem. Int. Ed. Engl. 41 2002 115 117 (Pubitemid 34076118)
40. Wilds C.J., Maier M.A., Manoharan M., and Egli M. Structural basis for recognition of guanosine by a synthetic tricylic cytosine analogue: guanidinium G-clamp Helv. Chim. Acta 86 2003 966 978 (Pubitemid 36644458)
41. Stengel G., Purse B.W., Wilhelmsson L.M., Urban M., and Kuchta R.D. Ambivalent incorporation of the fluorescent cytosine analogues tC and tCo by human DNA polymerase alpha and Klenow fragment Biochemistry 48 2009 7547 7555
42. Stengel G., Urban M., Purse B.W., and Kuchta R.D. Incorporation of the fluorescent ribonucleotide analogue tCTP by T7 RNA polymerase Anal. Chem. 82 2010 1082 1089
43. Urban M., Joubert N., Purse B.W., Hocek M., and Kuchta R.D. Mechanisms by which human DNA primase chooses to polymerize a nucleoside triphosphate Biochemistry 49 2010 727 735
44. Miller H., and Grollman A.P. Kinetics of DNA polymerase I (Klenow fragment exo-) activity on damaged DNA templates: effect of proximal and distal template damage on DNA synthesis Biochemistry 36 1997 15336 15342 (Pubitemid 27527999)
45. Shibutani S., and Grollman A.P. On the mechanism of frameshift (deletion) mutagenesis in vitro J. Biol. Chem. 268 1993 11703 11710 (Pubitemid 23168120)
46. Kuchta R.D., Benkovic P., and Benkovic S.J. Kinetic mechanism whereby DNA polymerase I (Klenow) replicates DNA with high fidelity Biochemistry 27 1988 6716 6725
47. Tahmassebi D.C., and Millar D.P. Fluorophore-quencher pair for monitoring protein motion Biochem. Biophys. Res. Commun. 380 2009 277 280
48. Hori M., Yonekura S.I., Nohmi T., Gruz P., Sugiyama H., Yonei S., and Zhang-Akiyama Q.M. Error-prone translesion DNA synthesis by Escherichia coli DNA polymerase IV (DinB) on templates containing 1,2-dihydro-2-oxoadenine J. Nucleic Acids 2010 2010 807579
49. Yamada M., Nunoshiba T., Shimizu M., Gruz P., Kamiya H., Harashima H., and Nohmi T. Involvement of Y-family DNA polymerases in mutagenesis caused by oxidized nucleotides in Escherichia coli J. Bacteriol. 188 2006 4992 4995 (Pubitemid 43956097)
50. Urban M., Joubert N., Hocek M., Alexander R.E., and Kuchta R.D. Herpes simplex virus-1 DNA primase: a remarkably inaccurate yet selective polymerase Biochemistry 48 2009 10866 10881
51. Tissier A., McDonald J.P., Frank E.G., and Woodgate R. Poliota, a remarkably error-prone human DNA polymerase Genes Dev. 14 2000 1642 1650 (Pubitemid 30460913)
52. Einolf H.J., Schnetz-Boutaud N., and Guengerich F.P. Steady-state and pre-steady-state kinetic analysis of 8-oxo-7,8-dihydroguanosine triphosphate incorporation and extension by replicative and repair DNA polymerases Biochemistry 37 1998 13300 13312 (Pubitemid 28449575)
53. Lutz M.J., Held H.A., Hottiger M., Hubscher U., and Benner S.A. Differential discrimination of DNA polymerase for variants of the non-standard nucleobase pair between xanthosine and 2,4-diaminopyrimidine, two components of an expanded genetic alphabet Nucleic Acids Res. 24 1996 1308 1313
54. Jager S., Rasched G., Kornreich-Leshem H., Engeser M., Thum O., and Famulok M. A versatile toolbox for variable DNA functionalization at high density J. Am. Chem. Soc. 127 2005 15071 15082 (Pubitemid 41547373)
55. Thum O., Jager S., and Famulok M. Functionalized DNA: a new replicable biopolymer Angew. Chem. Int. Ed. Engl. 40 2001 3990 3993 (Pubitemid 33081779)
56. Kool E.T. Active site tightness and substrate fit in DNA replication Annu. Rev. Biochem. 71 2002 191 219 (Pubitemid 34800219)
57. Pata J. Structural diversity of the Y-family DNA polymerases Biochem. Biophys. Acta 1804 2010 1124 1135
58. Broyde S., Wang L., Rechkoblit O., Geacintov N.E., and Patel D.J. Lesion processing: high-fidelity versus lesion-bypass DNA polymerases Trends Biochem. Sci. 33 2008 209 219
59. Humphrey W., Dalke A., and Schulten K. VMD-Visual Molecular Dynamics J. Mol. Graphics 14 1996 33 38
60. Ling H., Sayer J.M., Plosky B.S., Yagi H., Boudsocq F., and Woodgate R. Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase Proc. Natl Acad. Sci. USA 101 2004 2265 2269 (Pubitemid 38269300)
61. 6-methylguanine and cytosine, but accurate bypass is preferred J. Biol. Chem. 282 2007 1456 1467 (Pubitemid 47076521)
62. 6-benzylguanine by Sulfolobus solfataricus DNA polymerase Dpo4: steady-state and pre-steady-state kinetics and X-ray crystallography of correct and incorrect pairing J. Biol. Chem. 282 2007 13573 13584 (Pubitemid 47100492)
63. Chandani S., Jacobs C., and Loechler E.L. Architecture of Y-family DNA polymerases relevant to translesion DNA synthesis as revealed in structural and molecular modeling studies J. Nucleic Acids 2010 2010 20
64. Boudsocq F., Iwai S., Hanaoka F., and Woodgate R. Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic pol eta Nucleic Acids Res. 29 2001 4607 4616 (Pubitemid 33095021)
65. Fujii S., and Fuchs R.P. Defining the position of the switches between replicative and bypass DNA polymerases EMBO J. 23 2004 4342 4352 (Pubitemid 39546171)
66. Carver T.E. Jr., Hochstrasser R.A., and Millar D.P. Proofreading DNA: recognition of aberrant DNA termini by the Klenow fragment of DNA polymerase I Proc. Natl Acad. Sci. USA 91 1994 10670 10674 (Pubitemid 24329060)
67. Johnson S.J., and Beese L.S. Structures of mismatch replication errors observed in a DNA polymerase Cell 116 2004 803 816 (Pubitemid 38410726)
68. Jarosz D.F., Cohen S.E., Delaney J.C., Essigmann J.M., and Walker G.C. A DinB variant reveals diverse physiological consequences of incomplete TLS extension by a Y-family DNA polymerase Proc. Natl Acad. Sci. USA 106 2009 21137 21142
69. Beuning P.J., Simon S.M., Godoy V.G., Jarosz D.F., and Walker G.C. Characterization of Escherichia coli translesion synthesis polymerases and their accessory factors Methods Enzymol. 408 2006 318 340
70. Sandin P., Lincoln P., Brown T., and Wilhelmsson L.M. Synthesis and oligonucleotide incorporation of fluorescent cytosine analogue tC: a promising nucleic acid probe Nat. Protoc. 2 2007 615 623 (Pubitemid 47040022)
71. Maniatis T., Fritsch E.F., and Sambrook J. Molecular Cloning: A Laboratory Manual 2nd edit. 1989 Cold Spring Harbor Laboratory Woodbury, NY
72. Segel I. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems 1993 Wiley-Interscience New York, NY
73. Favicchio R., Dragan A.I., Kneale G.G., and Read C. Fluorescence spectroscopy and anisotropy in the analysis of DNA-protein interactions T. Moss, B. Leblanc, DNA-Protein Interactions: Principles and Protocols 3rd edit. 2009 Springer Science + Business Media New York, NY
74. Motulsky H. Intuitive Biostatistics 1995 Oxford University Press New York, NY
75. Swillens S. Interpretation of binding curves obtained with high receptor concentrations: practical aid for computer analysis Mol. Pharmacol. 47 1995 1197 1203
76. Wilhelmsson L.M., Sandin P., Holmen A., Albinsson B., Lincoln P., and Norden B. Photophysical characterization of fluorescent DNA base analogue, tC J. Phys. Chem. B 107 2003 9094 9101